A Phytophthora palmivora Extracellular Cystatin-Like Protease Inhibitor Targets Papain to Contribute to Virulence on Papaya
Papaya fruits, stems, and leaves are rich in papain, a cysteine protease that has been shown to mediate plant defense against pathogens and insects. Yet the oomycete Phytophthora palmivora is a destructive pathogen that infects all parts of papaya plants, suggesting that it has evolved cysteine prot...
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| Published in | Molecular plant-microbe interactions Vol. 31; no. 3; pp. 363 - 373 |
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| Main Authors | , , , |
| Format | Journal Article |
| Language | English |
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01.03.2018
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| Abstract | Papaya fruits, stems, and leaves are rich in papain, a cysteine protease that has been shown to mediate plant defense against pathogens and insects. Yet the oomycete Phytophthora palmivora is a destructive pathogen that infects all parts of papaya plants, suggesting that it has evolved cysteine protease inhibitors to inhibit papain to enable successful infection. Out of five putative extracellular cystatin-like cysteine protease inhibitors (PpalEPICs) from P. palmivora transcriptomic sequence data, PpalEPIC8 appeared to be unique to P. palmivora and was highly induced during infection of papaya. Purified recombinant PpalEPIC8 strongly inhibited papain enzyme activity, suggesting that it is a functional cysteine protease inhibitor. Homozygous PpalEPIC8 mutants were generated using CRISPR/Cas9-mediated gene editing via Agrobacterium-mediated transformation (AMT). Increased papain sensitivity of in-vitro growth and reduced pathogenicity during infection of papaya fruits were observed for the mutants compared with the wild-type strain, suggesting that PpalEPIC8, indeed, plays a role in P. palmivora virulence by inhibiting papain. This study provided genetic evidence demonstrating that plant-pathogenic oomycetes secrete cystatins as important weapons to invade plants. It also established an effective gene-editing system for P. palmivora by the combined use of CRISPR/Cas9 and AMT, which is expected to be applicable to other oomycetes. |
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| AbstractList | Papaya fruits, stems, and leaves are rich in papain, a cysteine protease that has been shown to mediate plant defense against pathogens and insects. Yet the oomycete Phytophthora palmivora is a destructive pathogen that infects all parts of papaya plants, suggesting that it has evolved cysteine protease inhibitors to inhibit papain to enable successful infection. Out of five putative extracellular cystatin-like cysteine protease inhibitors (PpalEPICs) from P. palmivora transcriptomic sequence data, PpalEPIC8 appeared to be unique to P. palmivora and was highly induced during infection of papaya. Purified recombinant PpalEPIC8 strongly inhibited papain enzyme activity, suggesting that it is a functional cysteine protease inhibitor. Homozygous PpalEPIC8 mutants were generated using CRISPR/Cas9-mediated gene editing via Agrobacterium-mediated transformation (AMT). Increased papain sensitivity of in-vitro growth and reduced pathogenicity during infection of papaya fruits were observed for the mutants compared with the wild-type strain, suggesting that PpalEPIC8, indeed, plays a role in P. palmivora virulence by inhibiting papain. This study provided genetic evidence demonstrating that plant-pathogenic oomycetes secrete cystatins as important weapons to invade plants. It also established an effective gene-editing system for P. palmivora by the combined use of CRISPR/Cas9 and AMT, which is expected to be applicable to other oomycetes. Papaya fruits, stems, and leaves are rich in papain, a cysteine protease that has been shown to mediate plant defense against pathogens and insects. Yet the oomycete Phytophthora palmivora is a destructive pathogen that infects all parts of papaya plants, suggesting that it has evolved cysteine protease inhibitors to inhibit papain to enable successful infection. Out of five putative extracellular cystatin-like cysteine protease inhibitors (PpalEPICs) from P. palmivora transcriptomic sequence data, PpalEPIC8 appeared to be unique to P. palmivora and was highly induced during infection of papaya. Purified recombinant PpalEPIC8 strongly inhibited papain enzyme activity, suggesting that it is a functional cysteine protease inhibitor. Homozygous PpalEPIC8 mutants were generated using CRISPR/Cas9-mediated gene editing via Agrobacterium-mediated transformation (AMT). Increased papain sensitivity of in-vitro growth and reduced pathogenicity during infection of papaya fruits were observed for the mutants compared with the wild-type strain, suggesting that PpalEPIC8, indeed, plays a role in P. palmivora virulence by inhibiting papain. This study provided genetic evidence demonstrating that plant-pathogenic oomycetes secrete cystatins as important weapons to invade plants. It also established an effective gene-editing system for P. palmivora by the combined use of CRISPR/Cas9 and AMT, which is expected to be applicable to other oomycetes.Papaya fruits, stems, and leaves are rich in papain, a cysteine protease that has been shown to mediate plant defense against pathogens and insects. Yet the oomycete Phytophthora palmivora is a destructive pathogen that infects all parts of papaya plants, suggesting that it has evolved cysteine protease inhibitors to inhibit papain to enable successful infection. Out of five putative extracellular cystatin-like cysteine protease inhibitors (PpalEPICs) from P. palmivora transcriptomic sequence data, PpalEPIC8 appeared to be unique to P. palmivora and was highly induced during infection of papaya. Purified recombinant PpalEPIC8 strongly inhibited papain enzyme activity, suggesting that it is a functional cysteine protease inhibitor. Homozygous PpalEPIC8 mutants were generated using CRISPR/Cas9-mediated gene editing via Agrobacterium-mediated transformation (AMT). Increased papain sensitivity of in-vitro growth and reduced pathogenicity during infection of papaya fruits were observed for the mutants compared with the wild-type strain, suggesting that PpalEPIC8, indeed, plays a role in P. palmivora virulence by inhibiting papain. This study provided genetic evidence demonstrating that plant-pathogenic oomycetes secrete cystatins as important weapons to invade plants. It also established an effective gene-editing system for P. palmivora by the combined use of CRISPR/Cas9 and AMT, which is expected to be applicable to other oomycetes. |
| Author | Tian, Miaoying Gumtow, Rebecca Uchida, Janice Wu, Dongliang |
| Author_xml | – sequence: 1 givenname: Rebecca surname: Gumtow fullname: Gumtow, Rebecca organization: Department of Plant and Environmental Protection Sciences, University of Hawaii at Manoa, Honolulu, 96822, U.S.A – sequence: 2 givenname: Dongliang surname: Wu fullname: Wu, Dongliang organization: Department of Plant and Environmental Protection Sciences, University of Hawaii at Manoa, Honolulu, 96822, U.S.A – sequence: 3 givenname: Janice surname: Uchida fullname: Uchida, Janice organization: Department of Plant and Environmental Protection Sciences, University of Hawaii at Manoa, Honolulu, 96822, U.S.A – sequence: 4 givenname: Miaoying surname: Tian fullname: Tian, Miaoying organization: Department of Plant and Environmental Protection Sciences, University of Hawaii at Manoa, Honolulu, 96822, U.S.A |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/29068239$$D View this record in MEDLINE/PubMed |
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| Cites_doi | 10.1094/PHYTO-09-15-0243-RVW 10.1104/pp.106.090050 10.1006/fgbi.1997.1006 10.1128/EC.2.2.191-199.2003 10.4161/psb.6.1.14190 10.1126/science.1195203 10.1016/j.tim.2007.10.013 10.1016/0014-5793(91)80804-C 10.1002/cpmc.25 10.1046/j.1364-3703.2003.00191.x 10.1074/jbc.M400941200 10.1016/j.pbi.2007.04.017 10.1099/00221287-99-2-311 10.1111/j.1574-6968.2007.00786.x 10.1016/0378-1119(90)90452-W 10.1046/j.1365-313X.2003.01968.x 10.1186/s12866-016-0825-1 10.1093/nar/gnh110 10.1371/journal.pone.0175795 10.1146/annurev.py.26.090188.000421 10.1371/journal.pone.0154027 10.1007/s00425-011-1392-1 10.1038/nprot.2008.73 10.1371/journal.pone.0040915 10.1016/j.fgb.2008.05.009 10.1073/pnas.0809201106 10.1093/bioinformatics/btu031 10.1186/s12915-017-0379-1 10.1093/bioinformatics/btm404 10.1073/pnas.0709303105 10.1099/mgen.0.000033 10.1105/tpc.107.056325 10.1021/bi0006971 10.1038/nmeth.1701 10.1146/annurev-phyto-080615-095944 10.1094/MPMI-6-015 10.1146/annurev.phyto.44.070505.143436 10.1093/gbe/evx021 10.1038/srep24765 10.1104/pp.105.061226 10.1126/science.1111404 10.1126/science.1246300 10.1186/1471-2105-11-129 10.1104/pp.110.158030 10.1371/journal.pgen.1003233 10.1111/mpp.12318 10.1111/mpp.12190 10.1371/journal.ppat.1005874 10.1371/journal.ppat.1003177 10.1093/bioinformatics/bti263 10.1038/nature08358 |
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| SubjectTerms | cystatins enzyme activity gene editing homozygosity insects leaves mutants papain papayas pathogens Phytophthora palmivora stems transcriptomics virulence |
| Title | A Phytophthora palmivora Extracellular Cystatin-Like Protease Inhibitor Targets Papain to Contribute to Virulence on Papaya |
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